IL-15 superagonist-mediated immunotoxicity: Role of NK cells and IFN-γ

Journal of Immunology

Volumn 195, Issue 5, 2015, Pages 2353-2364

  Guo, Yin ^a   Luan, Liming ^a   Rabacal, Whitney ^a   Bohannon, Julia K ^a   Fensterheim, Benjamin A ^a   Hernandez, Antonio ^a   Sherwood, Edward R ^a  

^a VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD69 ANTIGEN; GAMMA INTERFERON; GRANZYME B; INTERLEUKIN 15; INTERLEUKIN 15 SUPERAGONIST; PERFORIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; GRANZYME; INTERLEUKIN 15 RECEPTOR ALPHA; LECTIN; LEUKOCYTE ANTIGEN; MULTIPROTEIN COMPLEX; T LYMPHOCYTE ANTIGEN;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD8+ T LYMPHOCYTE; CELL EXPANSION; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME SYNTHESIS; FEMALE; HYPOTHERMIA; IMMUNOTOXICITY; LIVER INJURY; LYMPHOCYTE FUNCTION; LYMPHOCYTE PROLIFERATION; MORTALITY; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; T CELL DEPLETION; T LYMPHOCYTE ACTIVATION; WEIGHT REDUCTION; ANIMAL; BODY TEMPERATURE; C57BL MOUSE; CELL PROLIFERATION; CYTOTOXICITY; DOSE RESPONSE; DRUG EFFECTS; FLOW CYTOMETRY; GENETICS; HUMAN; IMMUNOLOGY; KNOCKOUT MOUSE; LYMPHOCYTE ACTIVATION; METABOLISM;

ANIMALS; ANTIGENS, CD; ANTIGENS, DIFFERENTIATION, T-LYMPHOCYTE; BODY TEMPERATURE; CD8-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; CYTOTOXICITY, IMMUNOLOGIC; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; FLOW CYTOMETRY; GRANZYMES; HUMANS; INTERFERON-GAMMA; INTERLEUKIN-15; INTERLEUKIN-15 RECEPTOR ALPHA SUBUNIT; KILLER CELLS, NATURAL; LECTINS, C-TYPE; LYMPHOCYTE ACTIVATION; MICE, INBRED C57BL; MICE, KNOCKOUT; MULTIPROTEIN COMPLEXES; PERFORIN;

EID: 84940121794     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1500300     Document Type: Article

References (45)

1. Fehniger, T. A., and M. A. Caligiuri. 2001. Interleukin 15: biology and relevance to human disease. Blood 97: 14-32.
2. Ma, A., R. Koka, and P. Burkett. 2006. Diverse functions of IL-2, IL-15, and IL-7 in lymphoid homeostasis. Annu. Rev. Immunol. 24: 657-679.
3. Mattei, F., G. Schiavoni, F. Belardelli, and D. F. Tough. 2001. IL-15 is expressed by dendritic cells in response to type I IFN, double-stranded RNA, or lipopolysaccharide and promotes dendritic cell activation. J. Immunol. 167: 1179-1187.
4. Ahmad, R., J. Ennaciri, P. Cordeiro, S. El Bassam, and J. Menezes. 2007. Herpes simplex virus-1 up-regulates IL-15 gene expression in monocytic cells through the activation of protein tyrosine kinase and PKC z/l signaling pathways. J. Mol. Biol. 367: 25-35.
5. Kennedy, M. K., M. Glaccum, S. N. Brown, E. A. Butz, J. L. Viney, M. Embers, N. Matsuki, K. Charrier, L. Sedger, C. R. Willis, et al. 2000. Reversible defects in natural killer and memory CD8 T cell lineages in interleukin 15-deficient mice. J. Exp. Med. 191: 771-780.
6. Lodolce, J., P. Burkett, R. Koka, D. Boone, M. Chien, F. Chan, M. Madonia, S. Chai, and A. Ma. 2002. Interleukin-15 and the regulation of lymphoid homeostasis. Mol. Immunol. 39: 537-544.
7. Ahmad, A., R. Ahmad, A. Iannello, E. Toma, R. Morisset, and S. T. Sindhu. 2005. IL-15 and HIV infection: lessons for immunotherapy and vaccination. Curr. HIV Res. 3: 261-270.
8. Zanoni, I., R. Spreafico, C. Bodio, M. Di Gioia, C. Cigni, A. Broggi, T. Gorletta, M. Caccia, G. Chirico, L. Sironi, et al. 2013. IL-15 cis presentation is required for optimal NK cell activation in lipopolysaccharide-mediated inflammatory conditions. Cell Reports 4: 1235-1249.
9. Bachanova, V., and J. S. Miller. 2014. NK cells in therapy of cancer. Crit. Rev. Oncog. 19: 133-141.
10. Diab, A., A. D. Cohen, O. Alpdogan, and M. A. Perales. 2005. IL-15: targeting CD8+ T cells for immunotherapy. Cytotherapy 7: 23-35.
11. Cha, E., L. Graham, M. H. Manjili, and H. D. Bear. 2010. IL-7 + IL-15 are superior to IL-2 for the ex vivo expansion of 4T1 mammary carcinoma-specific T cells with greater efficacy against tumors in vivo. Breast Cancer Res. Treat. 122: 359-369.
12. Suck, G., V. Y. Oei, Y. C. Linn, S. H. Ho, S. Chu, A. Choong, M. Niam, and M. B. Koh. 2011. Interleukin-15 supports generation of highly potent clinicalgrade natural killer cells in long-term cultures for targeting hematological malignancies. Exp. Hematol. 39: 904-914.
13. Klebanoff, C. A., L. Gattinoni, D. C. Palmer, P. Muranski, Y. Ji, C. S. Hinrichs, Z. A. Borman, S. P. Kerkar, C. D. Scott, S. E. Finkelstein, et al. 2011. Determinants of successful CD8+ T-cell adoptive immunotherapy for large established tumors in mice. Clin. Cancer Res. 17: 5343-5352.
14. Yu, P., J. C. Steel, M. Zhang, J. C. Morris, and T. A. Waldmann. 2010. Simultaneous blockade of multiple immune system inhibitory checkpoints enhances antitumor activity mediated by interleukin-15 in a murine metastatic colon carcinoma model. Clin. Cancer Res. 16: 6019-6028.
15. Zhang, M., Z. Yao, S. Dubois, W. Ju, J. R. Muller, and T. A. Waldmann. 2009. Interleukin-15 combined with an anti-CD40 antibody provides enhanced therapeutic efficacy for murine models of colon cancer. Proc. Natl. Acad. Sci. USA 106: 7513-7518.
16. Capitini, C. M., T. J. Fry, and C. L. Mackall. 2009. Cytokines as adjuvants for vaccine and cellular therapies for cancer. Am. J. Immunol. 5: 65-83.
17. Alpdogan, O., J. M. Eng, S. J. Muriglan, L. M. Willis, V. M. Hubbard, K. H. Tjoe, T. H. Terwey, A. Kochman, and M. R. van den Brink. 2005. Interleukin-15 enhances immune reconstitution after allogeneic bone marrow transplantation. Blood 105: 865-873.
18. Forget, M. A., S. Malu, H. Liu, C. Toth, S. Maiti, C. Kale, C. Haymaker, C. Bernatchez, H. Huls, E. Wang, et al. 2014. Activation and propagation of tumor-infiltrating lymphocytes on clinical-grade designer artificial antigenpresenting cells for adoptive immunotherapy of melanoma. J. Immunother. 37: 448-460.
19. Conlon, K. C., E. Lugli, H. C. Welles, S. A. Rosenberg, A. T. Fojo, J. C. Morris, T. A. Fleisher, S. P. Dubois, L. P. Perera, D. M. Stewart, et al. 2015. Redistribution, hyperproliferation, activation of natural killer cells and CD8 T cells, and cytokine production during first-in-human clinical trial of recombinant human interleukin-15 in patients with cancer. J. Clin. Oncol. 33: 74-82.
20. Blaser, B. W., N. R. Schwind, S. Karol, D. Chang, S. Shin, S. Roychowdhury, B. Becknell, A. K. Ferketich, D. F. Kusewitt, B. R. Blazar, and M. A. Caligiuri. 2006. Trans-presentation of donor-derived interleukin 15 is necessary for the rapid onset of acute graft-versus-host disease but not for graft-versus-tumor activity. Blood 108: 2463-2469.
21. Chapoval, A. I., J. A. Fuller, S. G. Kremlev, S. J. Kamdar, and R. Evans. 1998. Combination chemotherapy and IL-15 administration induce permanent tumor regression in a mouse lung tumor model: NK and T cell-mediated effects antagonized by B cells. J. Immunol. 161: 6977-6984.
22. Castillo, E. F., S. W. Stonier, L. Frasca, and K. S. Schluns. 2009. Dendritic cells support the in vivo development and maintenance of NK cells via IL-15 transpresentation. J. Immunol. 183: 4948-4956.
23. Han, K. P., X. Zhu, B. Liu, E. Jeng, L. Kong, J. L. Yovandich, V. V. Vyas, W. D. Marcus, P. A. Chavaillaz, C. A. Romero, et al. 2011. IL-15:IL-15 receptor a superagonist complex: high-level co-expression in recombinant mammalian cells, purification and characterization. Cytokine 56: 804-810.
24. Mortier, E., T. Woo, R. Advincula, S. Gozalo, and A. Ma. 2008. IL-15Rα chaperones IL-15 to stable dendritic cell membrane complexes that activate NK cells via trans presentation. J. Exp. Med. 205: 1213-1225.
25. Rubinstein, M. P., M. Kovar, J. F. Purton, J. H. Cho, O. Boyman, C. D. Surh, and J. Sprent. 2006. Converting IL-15 to a superagonist by binding to soluble IL-15Rα. Proc. Natl. Acad. Sci. USA 103: 9166-9171.
26. Stoklasek, T. A., K. S. Schluns, and L. Lefrancois. 2006. Combined IL-15/IL-15Rα immunotherapy maximizes IL-15 activity in vivo. J. Immunol. 177: 6072-6080.
27. Epardaud, M., K. G. Elpek, M. P. Rubinstein, A. R. Yonekura, A. Bellemare-Pelletier, R. Bronson, J. A. Hamerman, A. W. Goldrath, and S. J. Turley. 2008. Interleukin-15/interleukin-15Rα complexes promote destruction of established tumors by reviving tumor-resident CD8+ T cells. Cancer Res. 68: 2972-2983.
28. Xu, W., M. Jones, B. Liu, X. Zhu, C. B. Johnson, A. C. Edwards, L. Kong, E. K. Jeng, K. Han, W. D. Marcus, et al. 2013. Efficacy and mechanism-of-action of a novel superagonist interleukin-15: interleukin-15 receptor aSu/Fc fusion complex in syngeneic murine models of multiple myeloma. Cancer Res. 73: 3075-3086.
29. Chang, C. M., C. H. Lo, Y. M. Shih, Y. Chen, P. Y. Wu, K. Tsuneyama, S. R. Roffler, and M. H. Tao. 2010. Treatment of hepatocellular carcinoma with adeno-associated virus encoding interleukin-15 superagonist. Hum. Gene Ther. 21: 611-621.
30. Cheng, L., X. Du, Z. Wang, J. Ju, M. Jia, Q. Huang, Q. Xing, M. Xu, Y. Tan, M. Liu, et al. 2014. Hyper-IL-15 suppresses metastatic and autochthonous liver cancers by promoting tumor-specific CD8 T cell responses. J. Hepatol. 61: 1297-1303.
31. Callahan, M. K., and J. D. Wolchok. 2013. At the bedside: CTLA-4-and PD-1-blocking antibodies in cancer immunotherapy. J. Leukoc. Biol. 94: 41-53.
32. Curran, M. A., W. Montalvo, H. Yagita, and J. P. Allison. 2010. PD-1 and CTLA-4 combination blockade expands infiltrating T cells and reduces regulatory T and myeloid cells within B16 melanoma tumors. Proc. Natl. Acad. Sci. USA 107: 4275-4280.
33. 2014. PD-1 inhibitor approved for melanoma. Cancer Discov. 4: 1249.
34. Fujisaki, H., H. Kakuda, N. Shimasaki, C. Imai, J. Ma, T. Lockey, P. Eldridge, W. H. Leung, and D. Campana. 2009. Expansion of highly cytotoxic human natural killer cells for cancer cell therapy. Cancer Res. 69: 4010-4017.
35. Williams, M. T., Y. Yousafzai, C. Cox, A. Blair, R. Carmody, S. Sai, K. E. Chapman, R. McAndrew, A. Thomas, A. Spence, et al. 2014. Interleukin-15 enhances cellular proliferation and upregulates CNS homing molecules in pre-B acute lymphoblastic leukemia. Blood 123: 3116-3127.
36. Mishra, A., S. Liu, G. H. Sams, D. P. Curphey, R. Santhanam, L. J. Rush, D. Schaefer, L. G. Falkenberg, L. Sullivan, L. Jaroncyk, et al. 2012. Aberrant overexpression of IL-15 initiates large granular lymphocyte leukemia through chromosomal instability and DNA hypermethylation. Cancer Cell 22: 645-655.
37. Berger, C., M. Berger, R. C. Hackman, M. Gough, C. Elliott, M. C. Jensen, and S. R. Riddell. 2009. Safety and immunologic effects of IL-15 administration in nonhuman primates. Blood 114: 2417-2426.
38. Waldmann, T. A., E. Lugli, M. Roederer, L. P. Perera, J. V. Smedley, R. P. Macallister, C. K. Goldman, B. R. Bryant, J. M. Decker, T. A. Fleisher, et al. 2011. Safety (toxicity), pharmacokinetics, immunogenicity, and impact on elements of the normal immune system of recombinant human IL-15 in rhesus macaques. Blood 117: 4787-4795.
39. Perera, P. Y., J. H. Lichy, T. A. Waldmann, and L. P. Perera. 2012. The role of interleukin-15 in inflammation and immune responses to infection: implications for its therapeutic use. Microbes Infect. 14: 247-261.
40. Schwartz, R. N., L. Stover, and J. Dutcher. 2002. Managing toxicities of highdose interleukin-2. Oncology 16: 11-20.
41. Hayakawa, Y., N. D. Huntington, S. L. Nutt, and M. J. Smyth. 2006. Functional subsets of mouse natural killer cells. Immunol. Rev. 214: 47-55.
42. de Rham, C., S. Ferrari-Lacraz, S. Jendly, G. Schneiter, J. M. Dayer, and J. Villard. 2007. The proinflammatory cytokines IL-2, IL-15 and IL-21 modulate the repertoire of mature human natural killer cell receptors. Arthritis Res. Ther. 9: R125.
43. Blank, C., A. Luz, S. Bendigs, A. Erdmann, H. Wagner, and K. Heeg. 1997. Superantigen and endotoxin synergize in the induction of lethal shock. Eur. J. Immunol. 27: 825-833.
44. Ito, H., N. Koide, F. Hassan, S. Islam, G. Tumurkhuu, I. Mori, T. Yoshida, S. Kakumu, H. Moriwaki, and T. Yokochi. 2006. Lethal endotoxic shock using α-galactosylceramide sensitization as a new experimental model of septic shock. Lab. Invest. 86: 254-261.
45. Sherwood, E. R., and T. Toliver-Kinsky. 2004. Mechanisms of the inflammatory response. Best Pract. Res. Clin. Anaesthesiol. 18: 385-405.